Pertanika J. Trop. Agric. Sci. 36 (S): 47 - 54 (2013)

TROPICAL AGRICULTURAL SCIENCE

Journal homepage: http://www.pertanika.upm.edu.my/

Reproductive Patterns of Cynopterus brachyotis (Dog-Faced Fruit Bat) in Bintulu, Sarawak

Ibrahim, A.1, Musa, N.1, Mohd Top, M.1 and Zakaria, M.2* 1Department of Forestry Science, Faculty of Agriculture and Food Sciences, Universiti Putra Malaysia, Bintulu Sarawak Campus, 97008 Bintulu, Sarawak, Malaysia 2Faculty of Forestry, Universiti Putra Malaysia, 43400 Serdang, Selangor, Malaysia

ABSTRACT Reproductive period is a critical phase for most living organism. However, the influence of environmental condition on the reproductive pattern of Chiroptera in Malaysia is not well studied. A study on the reproductive patterns of dog-faced fruit bat, Cynopterus brachyotis, was conducted at Universiti Putra Malaysia, Bintulu Campus, Sarawak. Bats were captured in a planted forest and mixed dipterocarp forest using mist-nets for a period of 14 months from January 2009 to February 2010. The reproductive status was determined based on morphology of the bats. Five (I-Minor testes enlargement, no epididymal distention, II- Testes at or near maximal enlargement, no epididymal distention, III-Testes regressed, cauda epididymal distented, IV-Testes not regressed, cauda epididymal distented and V-No testiscular or epididymal enlargement) and four (I-Possibility pregnant, II-Lactating, III-Post-lactating and IV-Not reproductively active) categories of the reproductive status were categorized for the male and female C. brachyotis, respectively. Bats reproduce at all time of the year and the peak periods are associated with the rainy seasons. The first peak of reproduction (pregnancy and lactation) occurred in January to April 2009 and second peak in June to November 2009. The highest frequency of pregnancy and lactation female coincided with the fruit abundance. The results indicated that C. brachyotis performed a non-seasonal reproductive pattern. The findings are important in understanding the reproductive biology of bats and in protecting this ecologically important and diverse group of mammals.

Keywords: Cynopterus brachyotis, fruit bat, planted ARTICLE INFO forest, reproduction Article history: Received: 13 August 2012 Accepted: 20 September 2012

E-mail address: [email protected] (Zakaria, M.) * Corresponding author

ISSN: 1511-3701 © Universiti Putra Malaysia Press Ibrahim, A., Musa, N., Mohd Top, M. and Zakaria, M.

INTRODUCTION population. If these man-made disturbances The environmental factors are known to prevail without any perturbation, it will lead affect the timing of reproduction in many to bats’ population being threatened with species of mammals including bats. In extinction due to habitat loss, decreasing bats, the reproductive cycles are affected food resources, pollution, deliberate killing by photoperiod, rainfall, food abundance, and loss of genetic diversity (Meffe et al., and temperature (Heideman, 2000). Most 1994). Therefore, a better knowledge on bat species that have been studied to date the reproductive biology is important in the display strong seasonality and synchrony management and conservation of this diverse in their reproductive cycles such that group of mammals. This study was carried pregnancies and lactation coincide with food out to investigate the synchronization of the abundance. This increases the chances of the reproductive pattern between the male and young to survive. female C. brachyotis and to correlate it with The dog-faced fruit bat, Cynopterus the climatic and food availability factors. brachyotis (family Pteropodidae), is a common frugivorous species in Southeast MATERIALS AND METHODS Asia, and widely distributed in Malaysia. Study Site Throughout its range, this bat species This study was carried out in planted occupies a variety of habitats including forest (UPM~Mitsubishi Corporation primary forest, disturbed forest, mangrove, Forest Rehabilitation Research Project) cultivated areas, orchards, gardens, and (113o 03.591’ E, 03o 12.691’ N) and mixed urban areas (Funakoshi et al., 1997). Feeding dipterocarp forest (113o 04.105’ E, 03o areas and the composition of their food are 12.967’ N) at Universiti Putra Malaysia largely influenced by the seasonal flowering Bintulu Sarawak Campus (UPMKB) from and fruiting of trees (Kofron, 1997). The January 2009 to February 2010. species appears to be an important seed dispersal agent due to its wide distribution Bat Trapping and it is also important in pollination as it Cynopterus brachyotis were captured using feeds on nectar (Funakoshi et al., 1997). mist-nets that were set along the trails at the Considering its dependence on plants vicinity of flowering and fruiting trees and for food and the changing environment in open areas within the forest. Mist-nets (Funakoshi et al., 1997; Phua et al. 1989), were set up from dusk to dawn and checked the response of C. brachyotis to these factors at 10 pm and 5 am for 16 days every month and the timing of its reproduction are of for 14 months. All adult bats were recorded interest. and examined. Rising development in industries, The bats’ body mass (g), length of urbanization, animal husbandry and forearm (mm), sex, and their reproductive agriculture has been affecting bats’ status were determined. The reproductive

48 Pertanika J. Trop. Agric. Sci. 36 (S) 47 - 54 (2013) Reproductive Patterns of Cynopterus brachyotis (Dog-Faced Fruit Bat) in Bintulu, Sarawak status was assessed based on the morphology. RESULTS AND DISCUSSION The reproductive status was determined A total of 1,328 individual bats comprising following the characteristics outlined of 679 females and 649 males were trapped by Happold et al. (1990) and Kofron during the study period. The relationships (1997). Male bats were categorized into between body mass in male and female bats five reproductive status (I-Minor testes with rainfall, temperature and humidity over enlargement, no epididymal distention, 14 months from January 2009 to February II-Testes at or near maximal enlargement, 2010 are shown in Fig.1. Fig.2 shows no epididymal distention, III-Testes the male and female bats’ reproductive regressed, cauda epididymal distented, percentages for the 14 month’s period. Bats’ IV-Testes not regressed, cauda epididymal body mass was also used as an indirect distented and V-No testiscular or epididymal indicator of their reproductive status. The enlargement), while four reproductive status body mass of the male and female C. for female bats (I-Possibility pregnant, brachyotis fluctuated throughout the study II-Lactating, III-Post-lactating and IV-Not period. The highest male bats’ body mass reproductively active). Males with testes was recorded in January 2009 (33.15 ± 6.68 enlarged and females that were pregnant, g), whereby it coincided with the highest lactating and post-lactating were classified rainfall (1199.4 mm/month). Food resources as reproductively active individuals (Kofron, are more abundant in the rainy season than 1997). Meanwhile, post-lactating females in the dry season (Bumrungsri et al., 2007). possessed large, flaccid and dark nipples. The highest percentage (24.24%) of status II Females lacking these characteristics were (testes at or near maximal enlargement, no considered as non-reproductive (Duarte et epididymal distention) was recorded within al., 2010). this wet season (see Fig.2). Monthly climatic data were obtained In Myotis myotis, fluctuation of body from Bintulu Meteorology Station, Sarawak. mass can indicate times of food abundance Opportunistic observations on flowering and and scarcity (Andreas et al., 2007). During fruiting trees (in campus and study area) spermatogenesis of Pteropus poliocephalus, were also recorded monthly. Statistical the size of the testis increases to indicate tests were done using analysis of variance the time of reproduction (McGuckin et al., (ANOVA) to determine the difference in 1991). The testis size of C. brachyotis was body mass in different months. In addition, enlarged in January 2009, February 2009, Pearson’s correlation analysis was done to July 2009, August 2009, November 2009 determine whether there is a correlation and December 2009. This was synchronized between the male and female bats’ body with the increase of the body mass of mature mass with the climatic factors (rainfall, males, which might be influenced by the humidity and temperature). higher food availability (Table 1). According to Tan et al. (1998), C. brachyotis preferred

Pertanika J. Trop. Agric. Sci. 36 (S): 47 - 54 (2013) 49 Ibrahim, A., Musa, N., Mohd Top, M. and Zakaria, M.

Fig.1: The relationship between the male and female bats’ body mass (g) with rainfalls (mm), temperature (o C) and humidity (%) from January 2009 to February 2010 [this study is based on 1328 captures of adult C. brachyotis (male: 51 ± 21.09, female 52 ± 19.74 individuals caught each month)]. to feed on various kinds of non-seasonal which have caused the increase in body fruit. mass. Even though the highest female A study in the testes mass of C. brachyotis body mass was recorded in February 2009, showed that the peak mass occurred twice the peak of pregnant females (status I) in a year (from June to August and from (66.67%) was found to be synchronized with December to January) (Marina et al., 2002). the highest rainfall (see Fig.3). Therefore, Meanwhile, a study by Wong et al. (2002) rainfall is probably the most important showed that spermatogenesis occurred factor in the seasonal reproduction of throughout the year in the population but C. brachyotis. A study by Zortea (2003) peaked in the fruiting seasons. indicated that pregnancy peak in Anoura The highest females body mass was geoffroyi, A. caudifera and Glossophaga recorded in February 2009 (33.65 ± 5.85 soricina occurred in the rainy season. g), which occurred a month after the highest Food resources are more abundant in rainfall and the highest male body mass. the rainy season than in the dry season. This could be due to the gestation periods Pregnancy, lactation and weaning are the

50 Pertanika J. Trop. Agric. Sci. 36 (S) 47 - 54 (2013) Reproductive Patterns of Cynopterus brachyotis (Dog-Faced Fruit Bat) in Bintulu, Sarawak

Fig.2: The male (♂) and female (♀) bats’ reproductive status (%) for fourteen (14) months period. For male bats: I-Minor testes enlargement, no epididymal distention, II-Testes at or near maximal enlargement, no epididymal distention, III-Testes regressed, cauda epididymal distented, IV-Testes not regressed, cauda epididymal distented and V-No testiscular or epididymal enlargement. For female bats: I-Possibility pregnant, II-Lactating, III-Post-lactating and IV-Not reproductively active. most energetically reproductive stages; to April and August (Bumrungsri et al. therefore, they should coincide with the 2006), which is similar to the present study. period of high food availability (Racey, Based on opportunistic observation 1982). Although the highest monthly (Table 1), the fruiting seasons were captures of pregnant females occurred in recorded in January to February 2009 certain months (e.g., January to March 2009 (Mangifera indica, Fragrea fragrans) and June to November 2009), pregnant and June to October 2009 (Nephelium females were captured every month, lappaceum, Durio zibethinus, Mangifera suggesting that the breeding pattern is non- indica, Fragrea fragrans, Artocarpus seasonal. Compared to pregnant females, the integer). The non-seasonal fruiting trees, lactating females (status II) showed higher such as Ficus sp., show continuous fruit captures in April 2009 (21.21%) and August availability throughout the year, as shown 2009 (18.18%), suggesting that parturition by other studies (e.g. Wong et al., 2003; had occurred. Interestingly in Thailand, the Funakoshi et al., 1997; Lim (1970). Lim birth periods of C. brachyotis was in March (1970) found peaks in pregnancies to occur

Pertanika J. Trop. Agric. Sci. 36 (S): 47 - 54 (2013) 51 Ibrahim, A., Musa, N., Mohd Top, M. and Zakaria, M.

TABLE 1 The fruiting and flowering trees in Bintulu (through opportunistic observations)

Month Flowering and fruiting trees in Bintulu January 2009 Dipterocarp trees flowering Mangifera indica (mango), Artocarpus integer (cempedak), Fragrea fragrans (tembusu), Durio zibetinus (durian) February 2009 Mangifera indica (mango), Artocarpus integer (cempedak), Fragrea fragrans (tembusu) March 2009 Musa sp. (pisang), Piper nigrum (lada hitam), Muntingia calabura (ceri), Mimusops elengi (tanjung), Carica papaya (betik) April 2009 Musa sp. (pisang), Piper nigrum (lada hitam), Muntingia calabura (ceri), Mimusops elengi (tanjung), Carica papaya (betik) May 2009 Musa sp. (pisang), Piper nigrum (lada hitam), Muntingia calabura (ceri), Mimusops elengi (tanjung), Carica papaya (betik) June 2009 Mangifera indica (mango) Durio zibetinus (durian), Nephelium lappaceum (rambutan), Artocarpus integer (cempedak), Fragrae fragrans (tembusu) July 2009 Mangifera indica (mango) Durio zibetinus (durian), Nephelium lappaceum (rambutan), Artocarpus integer (cempedak), Fragrae fragrans (tembusu) August 2009 Mangifera indica (mango) Durio zibetinus (durian), Nephelium lappaceum (rambutan), Artocarpus integer (cempedak), Fragrae fragrans (tembusu) September 2009 Durio zibetinus (durian), Nephelium maingayi (rambutan), Artocarpus integer (cempedak) October 2009 Durio zibetinus (durian), Nephelium maingayi (rambutan), Artocarpus integer (cempedak) November 2009 Dipterocarp trees flowering Shorea( sp.) Musa sp. (pisang), Piper nigrum (lada hitam), Muntingia calabura (ceri), Mimusops elengi (tanjung), Carica papaya (betik) December 2009 Musa sp. (pisang), Piper nigrum (lada hitam), Muntingia calabura (ceri), Mimusops elengi (tanjung), Carica papaya (betik) January 2010 Musa sp. (pisang), Piper nigrum (lada hitam), Muntingia calabura (ceri), Mimusops elengi (tanjung), Carica papaya (betik) February 2010 Musa sp. (pisang), Piper nigrum (lada hitam), Muntingia calabura (ceri), Mimusops elengi (tanjung), Carica papaya (betik) Note: Non-seasonal fruits area available throughout the year in January, May, and September and these was a continuous bimodal polyoestry with coincided with the fruit abundance. This postpartum oestrus. finding contradicts the results of Kofron The differences in the C. brachyotis’ (1997) in Brunei, Borneo and Bumrungsri reproductive pattern are generally associated et al. (2007) in Thailand, who found that with different latitudes, which have been the reproductive pattern of C. brachyotis found to cause seasonality of rainfall and

52 Pertanika J. Trop. Agric. Sci. 36 (S) 47 - 54 (2013) Reproductive Patterns of Cynopterus brachyotis (Dog-Faced Fruit Bat) in Bintulu, Sarawak

Fig.3: The reproductive status of female Cynopterus brachyotis in relation to rainfall pattern from January 2009 to February 2010. food availability (Racey et al., 2000). CONCLUSION Only the male bats’ body mass showed In conclusion, the reproductive pattern of significant correlation (p<0.05) with the the important seed disperser C. brachyotis climatic factors (rainfall, temperature and is non-seasonal and significant correlation humidity). Kofron (1997) reported that only occurs between male bats’ body mass the increase/decrease of adult males’ body and climatic factor. In-depth information of mass for C. brachyotis corresponded with the reproductive pattern of the species will the bimodal cycle of ripened mangoes in help promote its protection in the forest. Brunei. However, the increase/decrease adult female C. brachyotis’ body mass ACKNOWLEDGEMENTS did not correspond to the bimodal cycle of The authors acknowledge the financial ripened mangoes. The results suggest that support provided by Universiti Putra male bats have to gain more energy for Malaysia~Mitsubishi Corporation Forest the mating repertoire (vocalizations, body Rehabilitation Research Project No. movement, special flight patterns, roost 6380500. defence, urinary tract markings), which is to pursuit the female partners. On the other REFERENCES hand, the body mass of female bats will Andreas, Z., Luisa, R., Ana, R., & Palmeirim, J. M. increase due to pregnancy. (2007). Critical times of the year for Myotis myotis, a temperate zone bat: roles of climate and food resources. Acta Chiropterologica, 9(1), 115–125.

Pertanika J. Trop. Agric. Sci. 36 (S): 47 - 54 (2013) 53 Ibrahim, A., Musa, N., Mohd Top, M. and Zakaria, M.

Anu, A., Sabu, T. K., & Vineesh, P. J. (2009). and P. scapulatus). Journal of Reproduction and Seasonality of litter insects and relationship with Fertility, 92, 339-346. rainfall in a wet evergreen forest in south Western Meffe, G. K., & Carroll, C. R. (1994). Principles Ghats. Journal of Insect Science, 72(2), 10-11. of conservations biology. Sunderland: Sinauer Bumrungsri, S., Bumrungsri, W., & Racey, P. A. Associates Inc., London. (2007). Reproduction in the short-nosed fruit bat Phua, P. B., & Corlett, R. (1989). Seed dispersal by in relation to environmental factors. Journal of the lesser short-nosed fruit bat (Cynopterus Zoology, 272, 73-81. brachyotis, Pteropodidae, Megachiroptera). Duarte, A. P. G., & Talamoni, S. A. (2010). Malayan Nature Journal, 42, 251-256. Reproduction of the large fruit-eating bat Racey, P. A. (1982). Ecology of bat reproduction. In Artibeus lituratus (Chiroptera: Phyllostomidae) T. H. Kunz (Ed.), Ecology of bats (p. 425). New in a Brazilian Atlantic forest area. Mammalian York: Plenum Press. Biology, 75(4), 320-325. Racey, P. A. (1988). Reproductive assessment in bats. Funakoshi, K., & Zubaid, A. (1997). Behavioral and In T. H. Kunz (Ed.), Ecological and Behavioral reproductive ecology of the dog-faced fruit bats, Methods in the Study of Bats (pp. 31–45). Cynopterus brachyotis and C. horsfieldi, in a Washington, D.C.: Smithsonian Institution Press. Malaysian rainforest. Mammal Study, 22, 95-108. Racey, P. A., & Entwistle, A. C. (2000). Life Happold, D. C. D., & Happold, M. (1990). history and reproductive strategies of bat. In Reproductive strategies of bats in Africa. Journal E.G. Crichton, & P. H. Krutzsch (Eds.), The of Zoology (London), 222, 557-583. reproductive biology of bats (pp. 469-499). Heideman, P. D. (2000). Environmental regulation of London: Academic Press. reproduction. In E. G. Crichton, & P. H. Krutzsch Wong, C. H., Tay, T. W., Marina, M. T., Zubaid, (Eds.), The reproductive biology of bats (pp. 469- A., & Kamis, A. B. (2001). Reproduction 499). London: Academic Press. Status of Male Cynopterus Brachyotis in an Kofron, C. P. (1997). Reproductive of two spesies of Agricultural Area and a Fragmented Forest. In congeneric fruit bats (Cynopterus) in Brunei. 12th International Bat Research Conference. 5-9th Journal of Zoology (London), 243, 485-506. August 2001, Bangi, Selangor, Malaysia.

Lim, B. L. (1970). Food habits and breeding cycle Wong, C. H., Tay, T. W., Marina, M. T., Zubaid, A., of the Malaysian fruit-eating bat, Cynopterus & Kamis, A. B. (2003). Male reproductive status brachyotis. Journal of Mammalogy, 51, 174-177. and testosterone concentration of Cynopterus brachyotis in a fragmented forest. Natural Marina, M. T., Wong, C. H., Tay, T. W., Zubaid, A., Resources Journal 31(2), 215-218. & Kamis, A. B. (2002). Annual changes in testes mass in Hipposideros larvatus, Cynopterus Zortea, M. (2003). Reproductive patterns and brachyotis and C. horsfieldi (Chiroptera) from feeding habits of three nectarivorous bats Peninsular Malaysia. Malaysian Applied Biology, (Phyllostomidae: Glossophaginae) from the 31(2), 85-86. Brazilian Cerrado. Brazilian Journal of Biology, 63(1), 159-168. McGuckin, M. A., & Blackshaw, A. W. (1991). Seasonal changes in testicular size, plasma testosterone concentration and body weight in captive flying foxes (Pteropus poliocephalus

54 Pertanika J. Trop. Agric. Sci. 36 (S) 47 - 54 (2013)